Type I Interferon Upregulates Bak and Contributes to T Cell Loss during Human Immunodeficiency Virus (HIV) Infection

PLoS Pathogens

Volumn 9, Issue 10, 2013, Pages

  Fraietta, Joseph A ^a   Mueller, Yvonne M ^a   Yang, Guibin ^a   Boesteanu, Alina C ^a   Gracias, Donald T ^a   Do, Duc H ^a   Hope, Jennifer L ^a   Kathuria, Noshin ^a   McGettigan, Shannon E ^b   Lewis, Mark G ^c   Giavedoni, Luis D ^d   Jacobson, Jeffrey M ^a   Katsikis, Peter D ^a  

^a DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c BIOQUAL INC   (United States)

^d SOUTHWEST NATIONAL PRIMATE RESEARCH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; BETA INTERFERON; BIM PROTEIN; FAS ANTIGEN; INTERFERON; PROTEIN BAK; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 9; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND;

ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL LOSS; CONTROLLED STUDY; DISEASE ASSOCIATION; EXPOSURE; FLOW CYTOMETRY; GENE EXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; MAJOR CLINICAL STUDY; MEMORY T LYMPHOCYTE; NONHUMAN; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RHESUS MONKEY; RNA INTERFERENCE; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; T LYMPHOCYTE; UPREGULATION; VIREMIA; VIRUS LOAD;

ADOLESCENT; ADULT; ANIMALS; ANTIGENS, CD95; APOPTOSIS; BCL-2 HOMOLOGOUS ANTAGONIST-KILLER PROTEIN; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CHILD; CHILD, PRESCHOOL; FEMALE; HIV INFECTIONS; HIV-1; HUMANS; IMMUNITY, CELLULAR; INFANT; INTERFERON-ALPHA; INTERFERON-BETA; MACACA MULATTA; MALE; TOLL-LIKE RECEPTOR 7; TOLL-LIKE RECEPTOR 9; UP-REGULATION; VIRAL LOAD; VIREMIA;

EID: 84887264025     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003658     Document Type: Article

References (76)

1. Finkel TH, Tudor-Williams G, Banda NK, Cotton MF, Curiel T, et al. (1995) Apoptosis occurs predominantly in bystander cells and not in productively infected cells of HIV- and SIV-infected lymph nodes. Nat Med 1: 129-134.
2. Gougeon ML, Garcia S, Heeney J, Tschopp R, Lecoeur H, et al. (1993) Programmed cell death in AIDS-related HIV and SIV infections. AIDS Res Hum Retroviruses 9: 553-563.
3. Meyaard L, Otto SA, Jonker RR, Mijnster MJ, Keet RP, et al. (1992) Programmed death of T cells in HIV-1 infection. Science 257: 217-219.
4. Gougeon ML, Lecoeur H, Dulioust A, Enouf MG, Crouvoiser M, et al. (1996) Programmed cell death in peripheral lymphocytes from HIV-infected persons: increased susceptibility to apoptosis of CD4 and CD8 T cells correlates with lymphocyte activation and with disease progression. J Immunol 156: 3509-3520.
5. Katsikis PD, Wunderlich ES, Smith CA, Herzenberg LA, (1995) Fas antigen stimulation induces marked apoptosis of T lymphocytes in human immunodeficiency virus-infected individuals. J Exp Med 181: 2029-2036.
6. Estaquier J, Idziorek T, Zou W, Emilie D, Farber CM, et al. (1995) T helper type 1/T helper type 2 cytokines and T cell death: preventive effect of interleukin 12 on activation-induced and CD95 (FAS/APO-1)-mediated apoptosis of CD4+ T cells from human immunodeficiency virus-infected persons. J Exp Med 182: 1759-1767.
7. Mueller YM, De Rosa SC, Hutton JA, Witek J, Roederer M, et al. (2001) Increased CD95/Fas-induced apoptosis of HIV-specific CD8(+) T cells. Immunity 15: 871-882.
8. Giorgi JV, Hultin LE, McKeating JA, Johnson TD, Owens B, et al. (1999) Shorter survival in advanced human immunodeficiency virus type 1 infection is more closely associated with T lymphocyte activation than with plasma virus burden or virus chemokine coreceptor usage. J Infect Dis 179: 859-870.
9. Mandl JN, Barry AP, Vanderford TH, Kozyr N, Chavan R, et al. (2008) Divergent TLR7 and TLR9 signaling and type I interferon production distinguish pathogenic and nonpathogenic AIDS virus infections. Nat Med 14: 1077-1087.
10. von Sydow M, Sonnerborg A, Gaines H, Strannegard O, (1991) Interferon-alpha and tumor necrosis factor-alpha in serum of patients in various stages of HIV-1 infection. AIDS Res Hum Retroviruses 7: 375-380.
11. Piasecki E, Knysz B, Gasiorowski J, Gladysz A, (1999) Decrease of enhanced interferon alpha levels in sera of HIV-infected and AIDS patients receiving combined antiretroviral therapy. Arch Immunol Ther Exp (Warsz) 47: 37-44.
12. Swindells S, Baldwin T, Kelly C, Baca-Regen L, Loomis L, et al. (1996) Regulation and characterization of the interferon-alpha present in patients with advanced human immunodeficiency virus type 1 disease. J Interferon Cytokine Res 16: 127-137.
13. Meylan PR, Guatelli JC, Munis JR, Richman DD, Kornbluth RS, (1993) Mechanisms for the inhibition of HIV replication by interferons-alpha,-beta, and-gamma in primary human macrophages. Virology 193: 138-148.
14. Cheney KM, McKnight A, (2010) Interferon-alpha mediates restriction of human immunodeficiency virus type-1 replication in primary human macrophages at an early stage of replication. PLoS One 5: e13521.
15. Luft T, Pang KC, Thomas E, Hertzog P, Hart DN, et al. (1998) Type I IFNs enhance the terminal differentiation of dendritic cells. J Immunol 161: 1947-1953.
16. Dondi E, Roue G, Yuste VJ, Susin SA, Pellegrini S, (2004) A dual role of IFN-alpha in the balance between proliferation and death of human CD4+ T lymphocytes during primary response. J Immunol 173: 3740-3747.
17. Hazenberg MD, Otto SA, van Benthem BH, Roos MT, Coutinho RA, et al. (2003) Persistent immune activation in HIV-1 infection is associated with progression to AIDS. AIDS 17: 1881-1888.
18. Deeks SG, Kitchen CM, Liu L, Guo H, Gascon R, et al. (2004) Immune activation set point during early HIV infection predicts subsequent CD4+ T-cell changes independent of viral load. Blood 104: 942-947.
19. Audige A, Urosevic M, Schlaepfer E, Walker R, Powell D, et al. (2006) Anti-HIV state but not apoptosis depends on IFN signature in CD4+ T cells. J Immunol 177: 6227-6237.
20. Lane HC, Davey V, Kovacs JA, Feinberg J, Metcalf JA, et al. (1990) Interferon-alpha in patients with asymptomatic human immunodeficiency virus (HIV) infection. A randomized, placebo-controlled trial. Ann Intern Med 112: 805-811.
21. Asmuth DM, Murphy RL, Rosenkranz SL, Lertora JJ, Kottilil S, et al. (2010) Safety, tolerability, and mechanisms of antiretroviral activity of pegylated interferon Alfa-2a in HIV-1-monoinfected participants: a phase II clinical trial. J Infect Dis 201: 1686-1696.
22. Kovacs JA, Bechtel C, Davey RT Jr, Falloon J, Polis MA, et al. (1996) Combination therapy with didanosine and interferon-alpha in human immunodeficiency virus-infected patients: results of a phase I/II trial. J Infect Dis 173: 840-848.
23. Jacquelin B, Mayau V, Targat B, Liovat AS, Kunkel D, et al. (2009) Nonpathogenic SIV infection of African green monkeys induces a strong but rapidly controlled type I IFN response. J Clin Invest 119: 3544-3555.
24. Keir ME, Rosenberg MG, Sandberg JK, Jordan KA, Wiznia A, et al. (2002) Generation of CD3+CD8low thymocytes in the HIV type 1-infected thymus. J Immunol 169: 2788-2796.
25. Herbeuval JP, Nilsson J, Boasso A, Hardy AW, Kruhlak MJ, et al. (2006) Differential expression of IFN-alpha and TRAIL/DR5 in lymphoid tissue of progressor versus nonprogressor HIV-1-infected patients. Proc Natl Acad Sci U S A 103: 7000-7005.
26. Fernandez S, Tanaskovic S, Helbig K, Rajasuriar R, Kramski M, et al. (2011) CD4+ T-cell deficiency in HIV patients responding to antiretroviral therapy is associated with increased expression of interferon-stimulated genes in CD4+ T cells. J Infect Dis 204: 1927-1935.
27. Baumler CB, Bohler T, Herr I, Benner A, Krammer PH, et al. (1996) Activation of the CD95 (APO-1/Fas) system in T cells from human immunodeficiency virus type-1-infected children. Blood 88: 1741-1746.
28. Boudet F, Lecoeur H, Gougeon ML, (1996) Apoptosis associated with ex vivo down-regulation of Bcl-2 and up-regulation of Fas in potential cytotoxic CD8+ T lymphocytes during HIV infection. J Immunol 156: 2282-2293.
29. Badley AD, Dockrell D, Simpson M, Schut R, Lynch DH, et al. (1997) Macrophage-dependent apoptosis of CD4+ T lymphocytes from HIV-infected individuals is mediated by FasL and tumor necrosis factor. J Exp Med 185: 55-64.
30. Petrovas C, Mueller YM, Dimitriou ID, Bojczuk PM, Mounzer KC, et al. (2004) HIV-specific CD8+ T cells exhibit markedly reduced levels of Bcl-2 and Bcl-xL. J Immunol 172: 4444-4453.
31. Arnoult D, Petit F, Lelievre JD, Lecossier D, Hance A, et al. (2003) Caspase-dependent and-independent T-cell death pathways in pathogenic simian immunodeficiency virus infection: relationship to disease progression. Cell Death Differ 10: 1240-1252.
32. David D, Keller H, Nait-Ighil L, Treilhou MP, Joussemet M, et al. (2002) Involvement of Bcl-2 and IL-2R in HIV-positive patients whose CD4 cell counts fail to increase rapidly with highly active antiretroviral therapy. AIDS 16: 1093-1101.
33. Roederer M, Dubs JG, Anderson MT, Raju PA, Herzenberg LA, (1995) CD8 naive T cell counts decrease progressively in HIV-infected adults. J Clin Invest 95: 2061-2066.
34. Beignon AS, McKenna K, Skoberne M, Manches O, DaSilva I, et al. (2005) Endocytosis of HIV-1 activates plasmacytoid dendritic cells via Toll-like receptor-viral RNA interactions. J Clin Invest 115: 3265-3275.
35. Meier A, Alter G, Frahm N, Sidhu H, Li B, et al. (2007) MyD88-dependent immune activation mediated by human immunodeficiency virus type 1-encoded Toll-like receptor ligands. J Virol 81: 8180-8191.
36. Hosmalin A, Lebon P, (2006) Type I interferon production in HIV-infected patients. J Leukoc Biol 80: 984-993.
37. Gorden KK, Qiu X, Battiste JJ, Wightman PP, Vasilakos JP, et al. (2006) Oligodeoxynucleotides differentially modulate activation of TLR7 and TLR8 by imidazoquinolines. J Immunol 177: 8164-8170.
38. Haas T, Metzger J, Schmitz F, Heit A, Muller T, et al. (2008) The DNA sugar backbone 2′ deoxyribose determines toll-like receptor 9 activation. Immunity 28: 315-323.
39. Gorden KK, Qiu XX, Binsfeld CC, Vasilakos JP, Alkan SS, (2006) Cutting edge: activation of murine TLR8 by a combination of imidazoquinoline immune response modifiers and polyT oligodeoxynucleotides. J Immunol 177: 6584-6587.
40. Fauci AS, Pantaleo G, Stanley S, Weissman D, (1996) Immunopathogenic mechanisms of HIV infection. Ann Intern Med 124: 654-663.
41. Grossman Z, Meier-Schellersheim M, Sousa AE, Victorino RM, Paul WE, (2002) CD4+ T-cell depletion in HIV infection: are we closer to understanding the cause? Nat Med 8: 319-323.
42. Gehri R, Hahn S, Rothen M, Steuerwald M, Nuesch R, et al. (1996) The Fas receptor in HIV infection: expression on peripheral blood lymphocytes and role in the depletion of T cells. AIDS 10: 9-16.
43. Salvato MS, Yin CC, Yagita H, Maeda T, Okumura K, et al. (2007) Attenuated disease in SIV-infected macaques treated with a monoclonal antibody against FasL. Clin Dev Immunol 2007: 93462.
44. Jeremias I, Herr I, Boehler T, Debatin KM, (1998) TRAIL/Apo-2-ligand-induced apoptosis in human T cells. Eur J Immunol 28: 143-152.
45. Herbeuval JP, Grivel JC, Boasso A, Hardy AW, Chougnet C, et al. (2005) CD4+ T-cell death induced by infectious and noninfectious HIV-1: role of type 1 interferon-dependent, TRAIL/DR5-mediated apoptosis. Blood 106: 3524-3531.
46. Miura Y, Misawa N, Maeda N, Inagaki Y, Tanaka Y, et al. (2001) Critical contribution of tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) to apoptosis of human CD4+ T cells in HIV-1-infected hu-PBL-NOD-SCID mice. J Exp Med 193: 651-660.
47. Katsikis PD, Garcia-Ojeda ME, Torres-Roca JF, Tijoe IM, Smith CA, et al. (1997) Interleukin-1 beta converting enzyme-like protease involvement in Fas-induced and activation-induced peripheral blood T cell apoptosis in HIV infection. TNF-related apoptosis-inducing ligand can mediate activation-induced T cell death in HIV infection. J Exp Med 186: 1365-1372.
48. de Oliveira Pinto LM, Garcia S, Lecoeur H, Rapp C, Gougeon ML, (2002) Increased sensitivity of T lymphocytes to tumor necrosis factor receptor 1 (TNFR1)- and TNFR2-mediated apoptosis in HIV infection: relation to expression of Bcl-2 and active caspase-8 and caspase-3. Blood 99: 1666-1675.
49. Herbein G, Van Lint C, Lovett JL, Verdin E, (1998) Distinct mechanisms trigger apoptosis in human immunodeficiency virus type 1-infected and in uninfected bystander T lymphocytes. J Virol 72: 660-670.
50. Shepard BD, De Forni D, McNamara DR, Foli A, Rizza SA, et al. (2008) Beneficial effect of TRAIL on HIV burden, without detectable immune consequences. PLoS One 3: e3096.
51. Chehimi J, Papasavvas E, Tomescu C, Gekonge B, Abdulhaqq S, et al. (2010) Inability of plasmacytoid dendritic cells to directly lyse HIV-infected autologous CD4+ T cells despite induction of tumor necrosis factor-related apoptosis-inducing ligand. J Virol 84: 2762-2773.
52. Thomas WD, Hersey P, (1998) TNF-related apoptosis-inducing ligand (TRAIL) induces apoptosis in Fas ligand-resistant melanoma cells and mediates CD4 T cell killing of target cells. J Immunol 161: 2195-2200.
53. Irmler M, Thome M, Hahne M, Schneider P, Hofmann K, et al. (1997) Inhibition of death receptor signals by cellular FLIP. Nature 388: 190-195.
54. Han J, Goldstein LA, Gastman BR, Rabinovitz A, Wang GQ, et al. (2004) Differential involvement of Bax and Bak in TRAIL-mediated apoptosis of leukemic T cells. Leukemia 18: 1671-1680.
55. McCloskey TW, Bakshi S, Than S, Arman P, Pahwa S, (1998) Immunophenotypic analysis of peripheral blood mononuclear cells undergoing in vitro apoptosis after isolation from human immunodeficiency virus-infected children. Blood 92: 4230-4237.
56. Lavrik IN, Krammer PH, (2012) Regulation of CD95/Fas signaling at the DISC. Cell Death Differ 19: 36-41.
57. Wei MC, Zong WX, Cheng EH, Lindsten T, Panoutsakopoulou V, et al. (2001) Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science 292: 727-730.
58. Wei MC, Lindsten T, Mootha VK, Weiler S, Gross A, et al. (2000) tBID, a membrane-targeted death ligand, oligomerizes BAK to release cytochrome c. Genes Dev 14: 2060-2071.
59. Petrovas C, Mueller YM, Dimitriou ID, Altork SR, Banerjee A, et al. (2007) Increased mitochondrial mass characterizes the survival defect of HIV-specific CD8(+) T cells. Blood 109: 2505-2513.
60. Petrovas C, Mueller YM, Katsikis PD, (2005) Apoptosis of HIV-specific CD8+ T cells: an HIV evasion strategy. Cell Death Differ 12 Suppl 1: 859-870.
61. Viollet L, Monceaux V, Petit F, Ho Tsong Fang R, Cumont MC, et al. (2006) Death of CD4+ T cells from lymph nodes during primary SIVmac251 infection predicts the rate of AIDS progression. J Immunol 177: 6685-6694.
62. Terawaki S, Chikuma S, Shibayama S, Hayashi T, Yoshida T, et al. (2011) IFN-alpha directly promotes programmed cell death-1 transcription and limits the duration of T cell-mediated immunity. J Immunol 186: 2772-2779.
63. Lederer S, Favre D, Walters KA, Proll S, Kanwar B, et al. (2009) Transcriptional profiling in pathogenic and non-pathogenic SIV infections reveals significant distinctions in kinetics and tissue compartmentalization. PLoS Pathog 5: e1000296.
64. Estaquier J, Idziorek T, de Bels F, Barre-Sinoussi F, Hurtrel B, et al. (1994) Programmed cell death and AIDS: significance of T-cell apoptosis in pathogenic and nonpathogenic primate lentiviral infections. Proc Natl Acad Sci U S A 91: 9431-9435.
65. Silvestri G, Sodora DL, Koup RA, Paiardini M, O'Neil SP, et al. (2003) Nonpathogenic SIV infection of sooty mangabeys is characterized by limited bystander immunopathology despite chronic high-level viremia. Immunity 18: 441-452.
66. Malleret B, Maneglier B, Karlsson I, Lebon P, Nascimbeni M, et al. (2008) Primary infection with simian immunodeficiency virus: plasmacytoid dendritic cell homing to lymph nodes, type I interferon, and immune suppression. Blood 112: 4598-4608.
67. Teijaro JR, Ng C, Lee AM, Sullivan BM, Sheehan KC, et al. (2013) Persistent LCMV infection is controlled by blockade of type I interferon signaling. Science 340: 207-211.
68. Wilson EB, Yamada DH, Elsaesser H, Herskovitz J, Deng J, et al. (2013) Blockade of chronic type I interferon signaling to control persistent LCMV infection. Science 340: 202-207.
69. Odorizzi PM, Wherry EJ, (2013) Immunology. An interferon paradox. Science 340: 155-156.
70. Parker R, Dutrieux J, Beq S, Lemercier B, Rozlan S, et al. (2010) Interleukin-7 treatment counteracts IFN-alpha therapy-induced lymphopenia and stimulates SIV-specific cytotoxic T lymphocyte responses in SIV-infected rhesus macaques. Blood 116: 5589-5599.
71. Vanderford TH, Slichter C, Rogers KA, Lawson BO, Obaede R, et al. (2012) Treatment of SIV-infected sooty mangabeys with a type-I IFN agonist results in decreased virus replication without inducing hyperimmune activation. Blood 119: 5750-5757.
72. Baum P, Fundel-Clemens K, Kreuz S, Kontermann RE, Weith A, et al. (2010) Off-target analysis of control siRNA molecules reveals important differences in the cytokine profile and inflammation response of human fibroblasts. Oligonucleotides 20: 17-26.
73. Lu W, Andrieu JM, (2001) In vitro human immunodeficiency virus eradication by autologous CD8(+) T cells expanded with inactivated-virus-pulsed dendritic cells. J Virol 75: 8949-8956.
74. Fraietta JA, Mueller YM, Do DH, Holmes VM, Howett MK, et al. (2010) Phosphorothioate 2′ deoxyribose oligomers as microbicides that inhibit human immunodeficiency virus type 1 (HIV-1) infection and block Toll-like receptor 7 (TLR7) and TLR9 triggering by HIV-1. Antimicrob Agents Chemother 54: 4064-4073.
75. Helbig KJ, Lau DT, Semendric L, Harley HA, Beard MR, (2005) Analysis of ISG expression in chronic hepatitis C identifies viperin as a potential antiviral effector. Hepatology 42: 702-710.
76. Giavedoni LD, (2005) Simultaneous detection of multiple cytokines and chemokines from nonhuman primates using luminex technology. J Immunol Methods 301: 89-101.